5 Condensed Tannins
Annual Plant Reviews book series, Volume 14: Plant Pigments and their Manipulation
Greg Tanner,
Greg Tanner
CSIRO Plant Industry, GPO Box 1600 Canberra ACT 2601, Australia
Search for more papers by this authorGreg Tanner,
Greg Tanner
CSIRO Plant Industry, GPO Box 1600 Canberra ACT 2601, Australia
Search for more papers by this authorThis article was originally published in 2004 in Plant Pigments and their Manipulation, Volume 14 (ISBN 9781405117371) of the Annual Plant Reviews book series, this volume edited by Kevin M. Davies. The article was republished in Annual Plant Reviews online in April 2018.
Abstract
The sections in this article are
- Introduction
- Biosynthesis from Coumaroyl-CoA to Leucoanthocyanidin
- Synthesis of Catechin (2,3-trans-flavan-3-ol)
- Synthesis of Epicatechin (2,3-cis-flavan-3-ol)
- Intravacuolar Transport and Polymerization
- Evolution of Biochemical Pathways
- Regulation of Biosynthesis
- Opportunities for Manipulation of Proanthocyanidins
- Conclusion
- Acknowledgments
References
- Aastrup, S., Outtrup, H. & Erdal, K. (1984) Location of the proanthocyanidins in the barley grain. Carlsberg Res. Comm., 49, 105–109.
- Abrahams, S., Lee, E., Walker, A. R., Tanner, G. J., Larkin, P. J. & Ashton, A. R. (2003) The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development. Plant Cell, 35, 624–636.
- Abrahams, S., Tanner, G. J., Larkin, P. J. & Ashton, A. R. (2002) Identification and biochemical characterization of mutants in the proanthocyanidin pathway in Arabidopsis. Plant Physiol., 130, 561–576.
- Aerts, R. J., Barry, T. N. & McNabb, W. C. (1999a) Polyphenols and agriculture: beneficial effects of proanthocyanidins in forages. Agric. Ecosystems Environ., 75, 1–12.
- Albert, S., Delseny, M. & Devic, M. (1997) Banyuls, a novel negative regulator of flavonoid biosynthesis in the Arabidopsis seed coat. Plant J., 11, 289–299.
- Alfenito, M. R., Souer, E., Goodman, C. D., Buell, R., Mol, J., Koes, R. & Walbot, V. (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell, 10, 1135–1149.
- Asquith, T. N., Izuno, C. C. & Butler, L. G. (1983) Characterization of the condensed tannin (proanthocyanidin) from a Group II sorghum. J. Agric. Food Chem., 31, 1299–1303.
- Ayres, M. P., Clausen, T. P., MacLean, S. F., Redman, A. M. & Reichardt, P. B. (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology, 78, 1696–1712.
- Bais, H. P., Walker, T. S., Stermitz, F. R., Hufbauer, R. A. & Vivanco, J. M. (2002) Enantiomeric-dependant phytotoxic and antimicrobial activity of (+)catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiol., 128, 1173–1179.
- Baker, M. E. & Blasco, R. (1992) Expansion of the mammalian 3β-hydroyysteroid dehydrogenase/plant dihydroflavonol reductase superfamily to include a bacterial cholesterol dehydrogenase, a bacterial UDP-galactose-4-epimerase, and open reading frames in vaccinia virus and fish lymphocystis disease virus. FEBS Lett., 301, 89–93.
- Barry, T. N. & Reid, C. S. W. (1985) Nutritional effects attributable to condensed tannins, cyanogenic glycosides and oestrogenic compounds in New Zealand forages, in Forage Legumes for Energy-Efficient Animal Production (eds R. F. Barnes, P. R. Ball, P. R. Brougham, G. G. Martin & D. J. Minson), USDA Agricultural Research Service, Washington, USA, pp. 251–259.
- Bavage, A. D., Davies, I. G., Robbins, M. P. & Morris, P. (1997) Expression of an Antirrhinum dihydroflavonol reductase gene results in changes in condensed tannin structure and accumulation in root cultures of Lotus corniculatus (bird's foot trefoil). Plant Mol. Biol., 35, 443–458.
- Bednar, R. A. & Hadcock, J. R. (1988) Purification and characterization of chalcone isomerase from soybeans. J. Biol. Chem., 263, 9582–9588.
- Berg, B. P., Majak, W., McAllister, T. A., Hall, J. W., McCartney, D., Coulman, B. E., Goplen, B. P., Acharya, S. N., Tait, R. M. & Cheng, K. J. (2000) Bloat in cattle grazing alfalfa cultivars selected for a low initial rate of digestion: a review. Can. J. Plant Sci., 80, 493–502.
- Bethke, P. C. & Jones, R. L. (2000) Vacuoles and provacuolar compartments. Curr. Opin. Plant Biol., 3, 469–475.
- Britsch, L., Dedio, J., Saedler, H. & Forkmann, G. (1993) Molecular characterization of flavanone 3 beta-hydroxylases. Consensus sequence, comparison with related enzymes and the role of conserved histidine residues. Eur. J. Biochem., 217, 745–754.
- Britsch, L. & Grisebach, H. (1986) Purification and characterization of (2S)-flavanone 3-hydroxylase from Petunia hybrida . Eur. J. Biochem., 156, 569–577.
- Britsch, L., Ruhnau-Brich, B. & Forkmann, G. (1992) Molecular cloning, sequence analysis, and in vitro expression of flavanone 3 beta-hydroxylase from Petunia hybrida . J. Biol. Chem., 267, 5380–5387.
- Brugliera, F., Barri-Rewell, G., Holton, T. A. & Mason, J. G. (1999) Isolation and characterization of a flavonoid 3′-hydroxylase cDNA clone corresponding to the Ht1 locus of Petunia hybrida . Plant J., 19, 441–451.
- Burbulis, I. E. & Winkel-Shirley, B. (1999) Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proc. Natl. Acad. Sci. USA, 96, 12929–12934.
- Cameron, A. R. & Malmo, J. (1993) A survey of the efficacy of sustained-release monensin capsules in the control of bloat in dairy cattle. Aust. Vet. J., 70, 1–4.
- Carron, T. R., Robbins, M. P. & Morris, P. (1994) Genetic modification of condensed tannin biosynthesis in Lotus corniculatus. 1. Heterologous antisense dihydroflavonol reductase down-regulates tannin accumulation in ‘hairy root’ cultures. Theor. Appl. Genet., 87, 1006–1015.
- Charrier, B., Coronado, C., Kondorosi, A. & Ratet, P. (1995) Molecular characterization and expression of alfalfa (Medicago sativa L.) flavanone-3-hydroxylase and dihydroflavonol-4-reductase encoding genes. Plant Mol. Biol., 29, 773–786.
- Clarke, R. T. J. & Reid, C. S. W. (1974) Foamy Bloat of Cattle. A review. J. Dairy Sci., 57 753–85.
- Consonni, G., Viotti, A., Dellaporta, S. L. & Tonelli, C. (1992) cDNA nucleotide sequence of Sn, a regulatory gene in maize. Nuc. Acids Res., 20, 373.
- Damiani, F., Paolocci, F., Cluster, P. D., Arcioni, S., Tanner, G. J., Joseph, R. G., Li, Y. G., deMajnik, J., & Larkin, P. J. (1999) The maize transcription factor Sn alters proanthocyanidin synthesis in transgenic Lotus corniculatus plants. Aust. J. Plant Physiol., 26, 159–169.
- Davies, K. M. (1993) A cDNA clone for flavanone 3-hydroxylase from Malus . Plant Physiol., 103, 291.
- Davin, L. B. & Lewis, N. G. (2000) Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignan and lignin biosynthesis. Plant Physiol., 123, 453–461.
- Debeaujon, I., Peeters, A. J. M., Leon-Kloosterziel, K. M. & Koorneef, M. (2001) The TRANSPARENT TESTA 12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell, 13, 853–871.
- Delcour, J. A., Ferreira, D. & Roux, D. G. (1983) Synthesis of condensed tannins. Part 9. The condensation sequence of leucocyanidin with (+)-catechin and with the resultant procyanidin. J. Chem. Soc. Perkin Trans. I, 1711–1717.
- de Majnik, J., Weinman, J. J., Djordjevic, M. A., Rolfe, B. G., Tanner, G. J., Joseph, R. G. & Larkin, P. J. (2000) Anthocyanin regulatory gene expression in transgenic white clover can result in an altered pattern of pigmentation. Aust. J. Plant Physiol., 27, 659–667.
- Deprez, S., Mila, I., Huneau, J. F., Tome, D. & Scalbert, A. (2001) Transport of proanthocyanidin dimer, trimer, and polymer across monolayers of human intestinal epithelial Caco-2 cells. Antioxid. Redox Signal., 3, 957–967.
- de Vetten, N., Horst, J. T., van Schaik, H. P., Boer, A. D., Mol, J. & Koes, R. (1999) A cytochrome b5 is required for full activity of flavonoid 3′,5′-hydroxylase, a cytochrome P450 involved in the formation of blue flower colors. Proc. Natl. Acad. Sci. USA, 96, 778–783.
- Devic, M., Guilleminot, J., Debeaujon, I., Bechtold, N., Bensaude, E., Koornneef, M., Pelletier, G. & Deiseny, M. (1999) The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. Plant J., 19, 387–398.
- Dixon, R. A., Blyden, E. R., Robbins, M. P., van Tunen, A. J. & Mol, J. N. (1988) Comparative biochemistry of chalcone isomerases. Phytochemistry, 27, 2801–2808.
- Dong, X. Y., Braun, E. L. & Grotewold. E. (2001) Functional conservation of plant secondary metabolic enzymes revealed by complementation of Arabidopsis flavonoid mutants with maize genes. Plant Physiol., 127, 46–57.
- Dooner, H. K., Robbins, T. P. & Jorgensen, R. A. (1991) Genetic and developmental control of anthocyanin biosynthesis. Ann. Rev. Genet., 25, 173–199.
- Doostdar, H., Shapiro, J. P., Niedz, R., Burke, M. D., McCollum, T. G., McDonald, R. E. & Mayer, R. T. (1995) A cytochrome P450 mediated naringenin 3′-hydroxylase from sweet orange cell cultures. Plant Cell Physiol., 36, 69–77.
- Downey, M. O., Harvey, J. S. & Robinson, S. P. ( 2003) Analysis of tannins in seeds and skins of Shiraz grapes throughout berry development. Aust. J. Grape Wine Res., 9, 15–27.
- Eckermann, S., Schroeder, G., Schimdt, J., Strack, D., Edrada, R. A., Helariutta, Y., Elomaa, P., Kotilainen, M., Kippelainen, I., Proksch, P., Teeri, T. H. & Schroder, J. (1998) New pathways to polyketides in plants. Nature, 396, 387–390.
- Erikson, A. J., Ramsewak, R. S., Smucker, A. J. & Nair, M. G. (2000) Nitrification inhibitors from roots of Leucaena leucocephala . J Agric. Food Chem., 48, 6174–6177.
-
Fay, M. F. & Dale, P. J. (1993) Condensed tannins in Trifolium species and their significance for taxonomy and plant breeding. Genet. Resour. Crop Evol., 40, 7–13.
10.1007/BF00053459 Google Scholar
-
Ferreira, D., Steynberg, J. P., Burger, J. F. W. & Bezuidenhoudt, B. C. B. (1992) Synthesis and base-catalysed transformations of proanthocyanidins, in Phenolic Metabolism in Plants (eds H. A. Stafford & R. K. Ibrahim), Plenum, New York, USA, pp. 255–295.
10.1007/978-1-4615-3430-3_9 Google Scholar
- Ferrer, J.-L., Jez, J. M., Bowman, M., Dixon, R. A. & Noel, J. P. (1999) Structure of chalcone synthase and the molecular basis of plant polyketide biosynthesis. Nat. Struct. Biol., 6, 775–784.
- Feucht, W., Treutter, D. & Christ, E. (1992) The precise localisation of catechins and proanthocyanidins in protective layers around fungal infections. J. Plant Dis. Protect., 99, 404–413.
- Fischer, D., Stich, K., Britsch, L. & Grisebach, H. (1988) Purification and characterization of (+)dihydroflavonol (3-hydroxyflavanone) 4-reductase from flowers of Dahlia variabilis . Arch. Biochem. Biophys., 264, 40–47.
- Fischer, T., Halbwirth, H., Meisel, B., Stich, K. & Forkmann, G. (2003) Molecular cloning, substrate specificity of the functionally expressed dihydroflavonol 4-reductases from Malus domestica, and Pyrus communis cultivars and the consequences for flavonoid metabolism. Arch. Biochem. Biophys., 412, 223–230.
- Foo, L. Y. & Porter, L. J. (1980) The phytochemistry of proanthocyanidin polymers. Phytochemistry, 19, 1747–1754.
-
Forkmann, G., Heller, W. & Grisebach, H. (1980) Anthocyanin biosynthesis in flowers of Matthiola incana flavanone 3- and flavonoid 3′-hydroxylases. Z. Naturforsch., C35, 691–695.
10.1515/znc-1980-9-1004 Google Scholar
-
Forkmann, G. (1993) Genetics of flavonoids, in The Flavonoids: Advances in Research Since 1986 (ed. J. B. Harborne), Chapman & Hall, London, UK, pp. 537–364.
10.1007/978-1-4899-2911-2_12 Google Scholar
- Frankel, E. N., Kanner, J., German, J. B., Parks, E. & Kinsella, J. E. (1993) Inhibition of oxidation of human low-density lipoprotein by phenolic substances in red wine. Lancet, 341, 454–457.
- Fritsch, H. & Grisebach, H. (1975) Biosynthesis of cyanidin in cell cultures of Haplopappas gracilis . Phytochemistry, 14, 2437–2442.
- Frova, C. (2003) The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol. Plant., 119, 469–479.
- Gang, D. R., Kasahara, H., Xia, Z.-Q., Mijnsbrugge, K. V., Bauw, G., Boerjan, W., Montagu, M. V., Davin, L. B. & Lewis, N. G. (1999) Evolution of plant defense mechanisms. J. Biol. Chem., 274, 7516–7527.
- Gong, Z. Z., Yamazaki, M., Sugiyama, M., Tanaka, Y. & Saito, K. (1997) Cloning and molecular analysis of structural genes involved in anthocyanin biosynthesis and expressed in a forma-specific manner in Perilla frutescens . Plant Mol. Biol., 35, 915–927.
- Goplen, B. P. (1989) Breeding bloat-safe alfalfa. Forage Focus, 2, 3.
- Goplen, B. P., Howarth, R. E., Sarkar, S. K. & Lesins, K. (1980) A search for condensed tannins in annual and perennial species of Mediago, Trigonella, & Onobrychis . Crop Sci., 20, 801–804.
- Grotewold, E. (2001) Subcellular trafficking of phytochemicals. Recent Res. Dev. Plant Physiol., 2, 31–48.
- Grotewold, E., Chamberlin, M., Snook, M., Siame, B., Butler, L., Swenson, J., Maddock, S., St-Clair, G. & Bowen, B. (1998) Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell, 10, 721–740.
- Grotewold, E., Drummond, B. J., Bowen, B. & Peterson, T. (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell, 76, 543–553.
- Hagermann, A. E. & Butler, L. G. (1981) The specificity of proanthocyanidin-protein interactions. J. Biol. Chem., 256, 4494–4497.
- Hagmann, M. L., Heller, W. & Grisebach, H. (1983) Induction and characterisation of a microsomal flavonoid 3′-hydroxylase from parsley cell cultures. Eur. J. Biochem., 134, 547–554.
- Halbwirth, H., Martens, S., Wienand, U., Forkmann, G. & Stich, K. (2003) Biochemical formation of anthocyanins in silk tissue of Zea mays . Plant Sci., 164, 489–495.
- Haslam, E. (1977) Review. Symmetry and promiscuity in procyanidin biochemistry. Phytochemistry, 16, 1625–1640.
- Hedqvist, H., Mueller-Harvey, I., Reed, J. D., Krueger, C. G. & Murphy, M. (2000) Characterisation of tannins and in vitro protein digestibility of several Lotus corniculatus varieties. Anim. Feed Sci. Tech., 87, 41–56.
-
Heller, W. & Forkmann, G. (1988) Biosynthesis, in The Flavonoids. Advances in Research Since 1980 (ed. J. B. Harborne), Chapman & Hall, London, UK, pp. 399–425.
10.1007/978-1-4899-2913-6_11 Google Scholar
-
Heller, W. & Forkmann, G. (1993) Biosynthesis of flavonoids, in The Flavonoids: Advances in Research Since 1986 (ed. J. B. Harborne), Chapman & Hall, London, UK, pp. 499–535.
10.1007/978-1-4899-2911-2_11 Google Scholar
- Hinz, G. & Herman, E. M. (2003) Sorting of storage proteins in the plant Golgi apparatus, in The Golgi Apparatus and the Plant Secretory Pathway (ed. D. G. Robinson), Blackwell, London, UK and CRC Press, Boca Raton, Florida, USA, pp. 141–164.
- Holton, T. A., Brugliera, F., Lester, D. R., Tanaka, Y., Hyland, C. D., Menting, J. G. T., Lu, C. Y., Farcy, E., Stevenson, T. W. & Cornish, E. C. (1993) Cloning and expression of cytochrome P450 genes controlling flower colour. Nature, 366, 276–279.
- Holton, T. A. & Cornish, E. C. (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell, 7, 1071–1083.
- Hrazdina, G. & Jensen, R. A. (1992) Spatial organisation of enzymes in plant metabolic pathways. Annu. Rev. Plant Physiol. Plant Mol. Biol., 43, 241–267.
- Ishikura, N., Murakami, H. & Fujii, Y. (1988) Conversion of (+)-dihydroquercetin to 3,4-cis-leucocyanidin by a reductase extracted from cell suspension cultures of Cryptomeria japonica . Plant Cell Physiol., 29, 795–799.
-
Jacques, D., Opie, C. T., Porter, L. J. & Haslam, E. (1977) Plant proanthocyanidins. Part 4. Biosynthesis of procyanidins and observations on the metabolism of cyanidin in plants. J. Chem. Soc. Perkin Trans.
I, 1637–1643.
10.1039/p19770001637 Google Scholar
- Jende-Strid, B. (1975) Mutations affecting flavonoid synthesis in barley, in Barley Genetics III. Proc. 3rd Int. Barley Genet. Sympos. Verlag Karl Thiemig, Munich, Germany, p. 36.
- Jende-Strid, B. (1993) Genetic control of flavonoid biosynthesis in barley. Hereditas, 119, 187–204.
- Jende-Strid, B. & Moller, B. L. (1981) Analysis of proanthocyanidins in wild-type and mutant barley (Hordeum vulgare L.). Carlsberg Res. Comm., 46, 53–64.
- Jez, J. M , Bowman, M. E., Dixon, R. A. & Noel, J. P. (2000) Structure and mechanism of the evolutionarily unique plant enzyme chalcone isomerase. Nat. Struct. Biol., 7, 786–791.
- Johnson, E. T., Ryu, S., Yi, H., Shin, B., Cheong, H. & Choi, G. (2001) Alteration of a single amino acid changes the substrate specificity of dihydroflavonol 4-reductase. Plant J., 25, 325–333.
- Jones, W. T. & Lyttleton, J. W. (1971) Bloat in cattle. XXXIV. A survey of legume forages that do and do not produce bloat. N. Z. J. Agric. Res., 14, 101–107.
- Jones, W. T. & Mangan, J. L. (1977) Complexes of the condensed tannins of sainfoin (Onobrychis viciifolia Scop.) with fraction 1 leaf protein and with submaxillary mucoprotein, and their reversal by polyethylene glycol and pH. J. Sci. Food Agric., 28, 126–136.
- Juah, G. Y., Phillips, T. E. & Rogers, J. C. (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell, 11, 1867–1882.
- Kaltenbach, M., Schroder, G., Schmelzer, E., Lutz, V. & Schroder, J. (1999) Flavonoid hydroxylase from Catharanthus roseus: cDNA, heterologous expression, enzyme properties and cell-type specific expression in plants. Plant J., 19 183–93.
- Keli, S. O., Hertog, M. G. L., Feskens, E. J. M. & Kromhout, D. (1996) Dietary flavonoids, antioxidant vitamins, and incidence of stroke. The Zutphen study. Arch. Intern. Med., 156, 637–642.
- Kennedy, J. A. & Jones, G. P. (2001) Analysis of proanthocyanidin cleavage products following acid-catalysis in the presence of excess phloroglucinol. J. Agric. Food Chem., 49, 1740–1746.
- Kitada, C., Gong, Z., Tanaka, Y., Yamazaki, M. & Saito, K. (2001) Differential expression of two cytochrome P450s involved in the biosynthesis of flavones and anthocyanins in chemo-varietal forms of Perilla frutescens . Plant Cell Physiol., 42, 1338–1344.
- Kitamura, S., Shikazono, N. & Tanaka, A. (2004) Transparent testa 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis . Plant J., 37, 104–114.
- Klein, M., Martinoia, E., Hoffmann-Thoma, G. & Weissenbock, G. (2000) A membrane-potential dependant ABC-like transporter mediates the vacuolar uptake of rye flavone glucuronides: regulation of glucuronide uptake by glutathione and its conjugates. Plant J., 21, 289–304.
- Koes, R. E., Quattrocchio, F. & Mol, J. N. M. (1994) The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays, 16, 123–132.
- Koornneef, M. (1990) Mutations affecting the testa colour in Arabidopsis. Arabid. Inf. Serv., 27, 1–4.
- Koupai-Abyazani, M. R., McCallum, J., Muir, A. D., Bohm, B. A., Towers, G. H. N. & Gruber, M. Y. (1993) Developmental changes in the composition of proanthocyanidins from leaves of sainfoin (Onobrychis viciifolia Scop.) as determined by HPLC analysis. J. Agric. Food Chem., 41, 1066–1070.
- Kraus, T. E. C., Dahlgren, R. A. & Zasoski, R. J. (2003) Tannins in nutrient dynamics of forest ecosystems: a review. Plant and Soil, 256, 41–66.
- Kreuzaler, F., Ragg, H., Fautz, E., Kuhn, D. N. & Hahlbrock, K. (1983) UV-induction of chalcone synthase mRNA in cell suspension cultures of Petroselinum hortense . Proc. Natl. Acad. Sci. USA, 80, 2591–2593.
- Kristiansen, K. N. (1984) Biosynthesis of proanthocyanidins in barley: genetic control of the conversion of dihydroquercetin to catechin and procyanidins. Carlsberg Res. Comm., 49, 503–524.
- Kristiansen, K. N. (1986) Conversion of (+)-dihydroquercetin to (+)-2,3-trans-3,4-cis-leucocyanidin and (+)-catechin with an enzyme extract from maturing grains of barley. Carlsberg Res. Comm., 51, 51–60.
- Labarbe, B., Cheynier, V., Broussaud, F., Souquet, J.-M. & Moutounet, M. (1999) Quantitative fractionation of grape proanthocyanidins according to their degree of polymerisation. J. Agric. Food Chem., 47, 2719–2723.
- Labesse, G., Vidal-Cros, A., Chomilier, J., Gaudry, M. & Mornon, J.-P. (1994) Structural comparisons lead to the definition of a new superfamily of NAD(P)(H)-accepting oxidoreductases: the single-domain reductases/ epimerases/ dehydrogenases (the ‘RED’ family). Biochem. J., 304, 95–99.
- Lancaster, J. E. (1992) Regulation of skin color in apples. Crit. Rev. Plant Sci., 10, 487–502.
- Larson, R. L. & Bussard, J. B. (1986) Microsomal flavonoid 3′-monooxygenase from maize seedlings. Plant Physiol., 80, 483–486.
- Lees, G. L., Gruber, M. Y. & Suttill, N. H. (1995) Condensed tannins in sainfoin. II. Occurrence and changes during leaf development. Can. J. Bot., 73, 1540–1547.
- Li, Y. G., Tanner, G. J., Delves, A. C. & Larkin, P. J. (1993) Asymmetric somatic hybrid plants between Medicago sativa L. (alfalfa, lucerne) and Onobrychis viciifolia Scop. (sainfoin). Theor. Appl. Genet., 87, 455–463.
- Li, Y. G., Tanner, G., & Larkin, P. (1996) The DMACA-HCl protocol and the threshold proanthocyanidin content for bloat safety in forage legumes. J. Sci. Food Agric., 70, 89–101.
- Li, Z.-S., Alfenito, M., Rea, P. A., Walbot, V., Dixon, R. A. & Li, Z. S. (1997) Vacuolar uptake of the phytoalexin medicarpin by the glutathione conjugate pump. Phytochemistry, 45, 689–693.
- Lu, Y. P., Li, Z. S. & Rea, P. A. (1997) AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. Proc Natl. Acad. Sci. USA, 94, 8243–8248.
- Ludwig, S. R., Habera, L. F., Dellaporta, S. L. & Wessler, S. R. (1989) Lc, a member of the maize R gene family responsible for tissue specific anthocyanin production, encodes a protein similar to transcription activators and contains the myc-homology region. Proc Natl. Acad. Sci. USA, 86, 7092–7096.
- Lukacin, R., Groning, I., Pieper, U. & Matern, U. (2000a) Site-directed mutagenesis of the active site serine290 in flavanone 3β-hydroxylase from Petunia hybrida . Eur. J. Biochem., 267, 853–860.
- Lukacin, R., Groning, I., Schiltz, E., Britsch, L. & Matern, U. (2000b) Purification of recombinant flavanone 3β-hydroxylase from Petunia hybrida and assignment of the primary site of proteolytic degradation. Arch Biochem. Biophys., 375, 364–370.
- Lukacin, R., Schreiner, S. & Matern, U. (2001) Transformation of acridone synthase to chalcone synthase. FEBS Lett., 508, 413–417.
- Lukacin, R., Urbanke, C., Groning, I. & Matern, U. (2000) The monomeric polypeptide comprises the functional flavanone 3β-hydroxylase from Petunia hybrida . FEBS Lett., 467, 353–358.
- Lukacin, R., Wellmann, F., Britsch, L., Martens, S. & Matern, U. (2003) Flavonol synthase from Citrus unshiu is a bifunctional dioxygenase. Phytochemistry, 62, 287–292.
- Markham, K. R., Tanner, G. J., Caasi-Lit, M., Whitecross, M. I., Nayudu, M. & Mitchell, K. A.(1998) Possible protective role for 3′,4′-dihydroxyflavones induced by enhanced UV-B in a UV-tolerant rice cultivar. Phytochemistry, 49, 1913–1919.
- Marles, M. A., Ray, H. & Gruber, M. Y. (2003) New perspectives on proanthocyanidin biochemistry and molecular regulation. Phytochemistry, 64, 367–383.
- Marshall, D. R., Broue, P. & Munday, J. (1979) Tannins in pasture legumes. Aust. J. Exp. Agric. Anim. Husb., 19, 192–197.
- Martin, C. & Gerats, T. (1993) The control of flower coloration, in The Molecular Biology of Flowering (ed. B. R. Jordan), CAB International, Wallingford, UK, pp. 219–255.
- Martin, C., Carpenter, R., Sommer, H., Saedler, H. & Coen, E. S. (1985) Molecular analysis of instability in flower pigmentation of Antirrhinum majus, following isolation of the pallida locus by transposon tagging. EMBO J., 4, 1625–1630.
- Martin, C., Prescott, A., Mackay, S., Bartlett, J. & Vrijlandt, E. (1991) Control of anthocyanin biosynthesis in flowers of Antirrhinum majus . Plant J., 1, 37–49.
- Meldgaard, M. (1992) Expression of chalcone synthase, dihydroflavonol reductase, and flavanone-3-hydroxylase in mutants of barley deficient in anthocyanin and proanthocyanidin biosynthesis. Theor. Appl. Genet., 83, 695–706.
- Menssen, A., Hohmann, S., Martin, W., Schnable, P. S., Peterson, P. A., Saedler, H. & Gierl, A. (1990) The En/Spm transposable element of Zea mays contains splice sites at the termini generating a novel intron from a dSpm element in the A2 gene. EMBO J., 9, 3051–3057.
- Menting, J. G. T., Scopes, R. K. & Stevenson, T. W. (1994) Characterization of flavonoid 3′,5′-hydroxylase in microsomal membrane fraction of Petunia hybrida flowers. Plant Physiol., 106, 633–642.
- Min, B. R., Barry, T. N., Attwood, G. T. & Mcnabb, W. C. (2003) The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Anim. Feed Sci. and Technology, 106, 3–19.
- Mol, J., Grotewold, E. & Koes, R. (1998) How genes paint flowers and seeds. Trends Plant Sci., 3, 212–217.
- Mol, J. N. M., Robbins, M. P., Dixon, R. A. & Veltkamp, E. (1985) Spontaneous and enzymatic rearrangement of naringenin chalcone to flavanone. Phytochemistry, 24, 2267–2269.
- Molan, A. L., Waghorn, G. C. & McNabb, W. C. (2002) Effect of condensed tannins on egg hatching and larval development of Trichostrongylus colubriformis in vitro . Vet. Rec., 150, 65–69.
- Morris, C. A., Cullen, N. G. & Geertsema, H. G. (1997) Genetic studies of bloat susceptibility in cattle. N. Z. Soc. Anim. Prod., 57, 19.
- Morris, P. & Robbins, M. P. (1997) Manipulating condensed tannins in forage legumes, in Biotechnology and the Improvement of Forage Legumes (eds B. D. McKersie & D. C. W. Brown), CAB International, Wallingford, UK, pp. 147–173.
- Mueller, L. A., Goodman, C. D., Silady, R. A. & Walbot, V. (2000) AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiol., 123, 1561–1570.
- Mueller, L. A., Walbot, V., Romeo, J. T., Saunders, J. A. & Matthews, B. F. (2001) Models for vacuolar sequestration of anthocyanins. Rec. Adv. Phytochem., 35, 297–312.
- Mueller, W. C. & Beckman, C. H. (1974) Ultrastructure of the phenol-storing cells in the roots of banana. Physiol. Plant Path., 4, 187–190.
- Nakajima, J.-I., Tanaka, Y., Yamazaki, M. & Saito, K. (2001) Reaction mechanism from leucoanthocyanidin to anthocyanidin 3-glucoside, a key reaction for coloring in anthocyanidin biosynthesis. J. Biol. Chem., 276, 25797–25803.
- Nielsen, K. M. & Podivinsky, E. (1997) cDNA cloning and endogenous expression of a flavonoid 3′5′-hydroxylase from petals of Lisianthus (Eustoma grandiflorum). Plant Sci., 129, 167–174.
- Northup, R. R., Yu, Z., Dahlgren, R.A. & Vogt, K. A. (1995) Polyphenol control of nitrogen release from pine litter. Nature, 377, 227–229.
- O'Reilly, C., Sheperd, N., Pereira, A., Schwarz-Somer, Z., Bertram, I., Robertson, D.S., Peterson, P.A. & Saedler, H. (1985) Molecular cloning of the A1 locus of Zea mays using the transposable elements En and Mul . EMBO J., 4, 877–882.
- Parham, R. A. & Kaustinen, H. M. (1977) On the site of tannin synthesis in plant cells. Bot. Gaz., 138, 465–467.
- Pelletier, M. K. & Shirley, B. W. (1996) Analysis of flavanone 3-hydroxylase in Arabidopsis seedlings. Coordinate regulation with chalcone synthase and chalcone isomerase. Plant Physiol., 111, 339–345.
- Polya, G. M. & Foo, L. Y. (1994) Inhibition of eukaryote signal-regulated protein kinases by plant-derived catechin-related compounds. Phytochemistry, 35, 1399–1405.
-
Porter, L. J. (1993) Flavans and proanthocyanidins, in The Flavanoids: Advances in Research Since 1986. (ed. J. B. Harbourne), Chapman & Hall, London, UK, pp. 23–55.
10.1007/978-1-4899-2911-2_2 Google Scholar
- Preisig-Mueller, R., Gehlert, R., Melchior, F., Stietz, U. & Kindl, H. (1997) Plant polyketide synthases leading to stilbenoids have a domain catalysing malonyl-CoA:CO2 exchange, malonyl-CoA decarboxylation, and covalent enzyme modification and a site for chain lengthening. Biochemistry, 36, 8349–8358.
-
Prescott, A. G. (2000) Two-oxoacid-dependant dioxygenases: inefficient enzymes or evolutionary driving force, in Evolution of Metabolic Pathways (eds J. T. Romeo, R. Ibrahim, L. Varin & V. deLuca), Pergamon, New York, USA, pp. 249–284.
10.1016/S0079-9920(00)80009-X Google Scholar
- Rausher, M. D., Miller, R. E. & Tiffin, P. (1999) Patterns of evolutionary rate variation among genes of the anthocyanin biosynthetic pathway. Mol. Biol. Evol., 16, 266–274.
- Ray, H., Yu, M., Auser, P., Blahut-Beatty, L., McKersie, B., Bowley, S., Westcott, N., Coulman, B., Lloyd, A. & Gruber, M. (2003) Expression of anthocyanins and proanthocyanidins after transformation of alfalfa with maize Lc . Plant Physiol., 132, 1448–1463.
- Reddy, A. R., Britsch, L., Salamini, F., Saedler, H. & Rohde, W. (1987) The A1 (anthocyanin-1) locus in Zea mays encodes dihydroquercetin reductase. Plant Sci., 52, 7–13.
- Reimold, U., Kroger, M., Kreuzaler, F. & Hahlbrock, K. (1983) Coding and 3' non-coding nucleotide sequence of chalcone synthase mRNA and assignement of amino acid sequence of the enzyme. EMBO J., 2, 1801–1805.
- Rizzi, M., Tonetti, M., Vigevani, P., Sturla, L., Bisso, A., de Flora, A., Bordo, D. & Bolognesi, M. (1998) GDP-4-keto-6-deoxy-D-mannose epimerase/reductase from Escherichia coli, a key enzyme in the biosynthesis of GDP-fucose, displays the structural characteristics of the RED protein homology superfamily. Structure, 6, 1453–1465.
- Robbins, M. P., Bavage, A. D., Strudwicke, C. & Morris, P. (1998) Genetic manipulation of condensed tannins in higher plants. II. Analysis of birdsfoot trefoil plants harboring antisense dihydroflavonol reductase constructs. Plant Physiol., 116, 1133–1144.
- Robbins, M. P., Paolocci, F., Hughes, J.-W., Turchette, V., Allison, G., Arcioni, S., Morris, P. & Damiani, F. (2003 ) Sn, a maize bHLH gene, modulates anthocyanin and condensed tannin pathways in Lotus corniculatus . J. Ex. Bot., 54, 239–248.
- Rumbaugh, M. D. (1979) The search for condensed tannins in the genus Medicago. Agronomy abstracts. Abstracts of 1979 annual meeting of American Society of Agronomy; Crop Science Society of America; and Soil Science Society of America; Fort Collins, Colorado, August 5–10, 1979, p. 75.
- Saito, K., Kobayashi, M., Gong, Z. Z., Tanaka, Y. & Yamazaki, M. (1999) Direct evidence for anthocyanidin synthase as a 2-oxoglutarate-dependant oxygenase: molecular cloning and functional expression of cDNA from a red forma of Perilla frutescens . Plant J., 17, 181–189.
-
Santos-Buelga, C. & Scalbert, A. (2000) Proanthocyanidins and tannin-like compounds – nature, occurence, dietary intake and effects on nutrition and health. J. Sci. Food Agric., 80, 1094–1117.
10.1002/(SICI)1097-0010(20000515)80:7<1094::AID-JSFA569>3.0.CO;2-1 CAS Web of Science® Google Scholar
- Saunders, C. M., Bonnett, S. L., Steynberg, J. P. & Ferreira, D. (1996) Oligomeric flavanoids. Part 24. Controlled biomimetic synthesis of profisetinidin triflavanoid related phlobatannins. Tetrahedron, 52, 6003–6010.
- Scalbert, A. (1991) Antimicrobial properties of tannins. Phytochemistry, 30, 3875–3883.
- Scalbert, A., Morand, C., Manach, C. & Remesy, C. (2002) Absorption and metabolism of polyphenols in the gut and impact on health. Biomedicine Pharmacotherapy, 56, 276–282.
- Schoenbohm, C., Martens, S., Eder, C., Forkmann, G. & Weisshaar, B. (2000) Identification of the Arabisopsis thaliania flavonoid 3′-hydroxylase gene and functional expression of the encoded P450 enzyme. Biol. Chem., 381, 749–753.
-
Schroder, J. (2000) The family of chalcone synthase-related proteins: functional diversity and evolution, in Evolution of Metabolic Pathways (eds J. T. Romeo, R. Ibrahim, L. Varin & V. deLuca), Pergamon, New York, USA, pp. 55–89.
10.1016/S0079-9920(00)80004-0 Google Scholar
- Schultz, J. C., Hunter, M. D. & Appel, H. M. (1992) Antimicrobial activity of polyphenols mediates plant-herbivore interactions, in Plant Polyphenols: Synthesis, Properties, Significance (eds R. W. Hemmingway, P. E. Laks & S. J. Branham), Plenum, New York, USA, pp. 621–637.
- Shimada, N., Aoki, T., Sato, S., Nakamura, Y., Tabata, S. & Ayabe, S. (2003) A cluster of genes encodes the two types of chalcone isomerase involved in the biosynthesis of general flavonoids and legume-specific 5-deoxy(iso)flavonoids in Lotus japonicus . Plant Physiol., 131, 941–951.
- Shimada, Y., Nakano-Shimada, R., Ohbayashi, M., Okinaka, Y., Kiyokawa, S. & Kikuchi, Y. (1999) Expression of chimeric P450 genes encoding flavonoid-3′5′-hydroxylase in transgenic tobacco and Petunia plants. FEBS Lett., 461, 241–245.
- Shirley, B. W., Kubasek, W. L., Storz, G., Bruggemann, E., Koornneef, M., Ausubel, F. M. & Goodman, H. M. (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J., 8, 659–671.
- Singh, S., McCallum, J., Gruber, M. Y., Towers, G. H. N., Muir, A. D., Bohm, B. A., Koupai-Abyazani, M. R., Glass, A. D. M. & Singh, S. (1997) Biosynthesis of flavan-3-ols by leaf extracts of Onobrychis viciifolia . Phytochemistry, 44, 425–432.
- Skadhauge, B., Gruber, M. Y., Thomsen, K. K., & von Wettstein, D. (1997a) Leucocyanidin reductase activity and accumulation of proanthocyanidins in developing legume tissues. Am. J. Bot., 84, 494–503.
- Skadhauge, B., Thomsen, K. K., & von Wettstein, D. (1997b) The role of the barley testa layer and its flavonoid content in resistance to Fusarium infections. Hereditas, 126, 147–160.
- Sparvoli, F., Martin, C., Scienza, A., Gavazzi, G. & Tonelli, C. (1994) Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Mol. Biol., 24, 743–755.
- Stafford, H. A. (1974) Possible multi-enzyme complexes regulating the formation of C6-C3 phenolic compounds and lignans in higher plants. Recent Adv. Phytochem., 8, 53–79.
- Stafford, H. A. (1990) Flavonoid metabolism, CRC Press, Boca Raton, Florida, USA.
-
Stafford, H. A. (2000) The evolution of phenolics in plants, in Evolution of Metabolic Pathways (eds J. T. Romeo, R. Ibrahim, L. Varin & V. deLuca), Pergamon, New York, USA, pp. 25–54.
10.1016/S0079-9920(00)80003-9 Google Scholar
- Stafford, H. A. & Lester, H. A. (1984) Flavan-3-ol biosynthesis. The conversion of (+)dihydroquercetin and flavav-3,4-cis-diol (leucocyanidin) to (+)-catechin by reductases extracted from cell suspension cultures of Douglas Fir. Plant Physiol., 76, 184–186.
- Stafford, H. A. & Lester, H. A. (1985) Flavan-3-ol biosynthesis: the conversion of (+)-dihydromyrecetin to its flavan-3,4-diol (leucodelphinidin) and to (+)-gallocatechin by reductases extracted from tissue cultures of Ginkgo biloba and Pseudotsuga menziesii . Plant Physiol., 78, 791–794.
- Stafford, H. A. & Lester, H. H. (1982) Enzymic and non-enzymic reduction of (+)-dihydroquercetin to its 3,4-diol. Plant Physiol., 70, 695–698.
- Stafford, H. A., Shimamoto, M. & Lester, H. H. (1982) Incorporation of [14C]phenylalanine into flavan-3-ols and procyanidins in cell suspension cultures of Douglas Fir. Plant Physiol., 69, 1055–1059.
- Stotz, G. & Forkmann, G. (1982) Hydroxylation of the B-ring of flavonoids in the 3′- and 5′-positions with enzyme extracts from flowers of Verbena hybrida . Z. Naturforsch., 37c, 19–23.
- Stotz, G., Spribille, R. & Forkmann, G. (1984) Flavonoid biosynthesis in flowers of Verbena hybrida . J. Plant Physiol., 116, 173–183.
- Tanaka, Y., Yonekura, K., Fukuchi-Mizutani, M., Fukui, Y., Fujiwara, H., Ashikari, T. & Kusumi, T. (1996) Molecular and biochemical characterization of three anthocyanin synthetic enzymes from Gentiana triflora . Plant Cell Physiol., 37, 711–716.
- Tanner, G. J., Abrahams, S. A. & Larkin, P. J. (2000) Biosynthesis of condensed tannins in cereals and other plants, in Tannins in Livestock and Human Nutrition (ed. J. D. Brooker), ACIAR, Canberra, http://www.aciar.gov.au/downloads/publications/tannins/TAN08BTA.PDF.
- Tanner, G. J., Francki, K. T., Abrahams, S., Watson, J. M., Larkin, P. J. & Ashton, A. R. (2003) Proanthocyanidin biosynthesis in plants. Purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. J. Biol. Chem., 278, 31647–31656.
- Tanner, G. J. & Kristiansen, K. N. (1993) Synthesis of 3,4,-cis-[3H]leucocyanidin and enzymatic reduction to catechin. Anal. Biochem., 209, 274–277.
- Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nuc. Acids Res., 22, 4673–4680.
- Toda, K., Yang, D., Yamanaka, N., Watanabe, S., Harada, K. & Takahashi, R. (2002) A single-base deletion in soybean flavonoid 3′-hydroxylase gene is associated with gray pubescence color. Plant Mol. Biol., 50, 187–196.
- Turnbull, J. J., Nagle, M. J., Seibel, J. F., Welford, R. W. D., Grant, G. & Schofield, C. J. (2003) The C-4 stereochemistry of leucocyanidin substrates for anthocyanidin synthase affects product selectivity. Bioorg. Med. Chem. Lett., 13, 3853–3857.
- Turnbull, J. J., Sobey, W. J., Alpin, R. T., Hassan, A., Firmin, J. L., Schofield, C. J. & Prescott, A. G. (2000) Are anthocyanidins the immediate products of anthocyanidin synthase? Chem. Commun., 24, 2473–2474.
- Turnbull, J. J., Prescott, A. G., Schofield, C. J. & Wilmouth, R. C. (2001) Purification, crystallization and preliminary X-ray diffraction of anthocyanidin synthase from Arabidopsis thaliana . Acta Cryst. Sec. D, Biol. Cryst., 57, 425–427.
- von Wettstein, D., Nilan, R. A., Ahrenst-Larsen, B. , Erdal, K., Ingversen, J., Jende-Strid, B., Kristiansen, K. N., Larsen, J., Outtrup, H. & Ullrich, S. E. (1985) Proanthocyanidin-free barley for brewing: progress in breeding for high yield and research tool in polyphenol chemistry. MBAA Tech. Quart., 22, 41–52.
- Welle, R., Schroder, G., Schiltz, E., Grisebach, H. & Schroder, J. (1991) Induced plant responses to pathogen attack. Analysis and heterologous expression of the key enzyme in the biosynthesis of phytoalexins in soybean (Glycine max L. Merr. cv. Harosoy 63). Eur. J. Biochem., 196, 423–430.
- Wellmann, F., Lukacin, R., Moriguchi, T., Britsch, L., Schiltz, E. & Matern, U. (2002) Functional expression and mutational analysis of flavonol synthase from Citrus unshiu . Eur. J. Biochem., 269, 4134–4142.
- Wilmouth, R., Turnbull, J. J., Welford, R. W. D., Clifton, I. J., Prescot, A. G. & Schofield, C. J. (2002) Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliania . Structure, 10, 93–103.
- Winkel-Shirley, B. (1999) Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol. Plant., 107, 142–149.
- Winkel-Shirley, B. (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol., 126, 485–493.
- Winkel-Shirley, B. (2002) Molecular genetics and control of anthocyanin expression, in Advances in Botanical Research (eds K. S. Gould, D. W. Lee, & J. A. Callow), Academic Press, London, UK, pp. 76–94.
- Wiseman, E., Hartmann, U., Sagasser, M., Baumann, E., Palme, K., Hahlbrock, K., Saedler, H. & Weisshaar, B. (1998) Knockout mutants from an En-1 mutagenised Arabidopsis thaliania population generate phenylpropanoid biosynthesis phenotypes. Proc. Natl. Acad. Sci. USA, 95, 12432–12437.
- Xie, D. Y., Sharma, S. B., Paiva, N. L., Ferreira, D. & Dixon, R. A. (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science, 299, 396–399.
Citing Literature
Browse other articles of this reference work: